Quantitation of in the Digits: A Psychophysical Study in Normal Human Subjects Emre Kokmen, MD, Robert W. Bossemeyer, Jr, MScEE, and William J. Williams, PhD

Threshold perception of motion of the digits was obtained in 14 normal subjects. The metacarpophalangeal joint of the index and the fifth finger of each hand and the metatarsophalangeal joint of the hallux of each foot were passively moved up and down with respect to a horizontal plane defined by the palmar or plantar surface. The motion was sinusoidal at frequencies of 0.5 and 5.0 Hz. A modified von Bekesy paradigm similar to that used in audiometry was utilized to yield threshold levels of motion sensation. There was little difference in the thresholds obtained for the different joints. The difference between high- and low-frequency stimulation, however, was significant (p < 0.001): the 0.5 Hz threshold was found to range from 0.8 to 1 .0 degree, whereas the 5.0 Hz threshold varied from 0.4 to 0.6 degree. It is thought that motion sense is largely dependent on joint receptor contributions, but muscle and cutaneous receptors may also contribute to this proprioceptive sensation.

Kokmen E, Bossemeyer RW Jr, Williams WJ. Quantitation of motion perception in the digits: a psychophysical study in normal human subjects. Ann Neurol 2:279-284, 1977

A number of efforts have been made in the past to studying the nature of proprioceptive sensations in quantitate somatic senses [5], including a few studies humans. Such a method can also be a useful tool in the which have attempted to measure perception of mo- longitudinal and comparative evaluation of patients tion of limbs or digits. In 1889 Goldscheider [8] with selected neurological conditions as well as in recorded perception of passive motion in several assessing sensory performance of selected popula- joints moved with an elaborate hydraulic system. tions, such as the aged versus the young. However, Laidlaw and Hamilton [14] moved joints passively before the method can be used in clinical studies, with a hand-cranked mechanical device. Browne, Lee, some normative values must be established. We re- and Ring [2] moved the metatarsophalangeal joint port the motion perception thresholds obtained in a (MTP) passively with a motor-driven assembly. The group of young, healthy naive subjects. subjects indicated perception by depressing a switch, causing the angle through which the digit had been Methods and Materials An electrically controlled mechanical system was developed moved to be recorded. Provins [20] used a similar to move the fingers and toes up and down and to articulate method to study the appreciation of index finger the MCP joint of the index and fifth finger of each hand and movements at the metacarpophalangeal (MCP) joint. the MTP joint of the hallux of each foot. In all cases, the A quantitative psychophysical evaluation is needed subject was completely relaxed and the movement of the to study the characteristics of motion perception in digit was passive. The finger or toe was placed in a padded humans. Bedside clinical sensory testing methods lack plastic clamp that held the digit firmly and prevented motion precise control of stimulation delivery and response of the distal interphalangeal joint. Since we were concerned recording and evaluation. The intensity, frequency, at the outset that differential pressures on the dorsal or direction, and sites of application of the stimuli must ventral surface of the digit might give motion clues, several be controlled, and responses of the subjects must be types of finger and toe holders, including one with an inflat- recorded consistently. able inner liner, were tried in preliminary experiments. The final model used in this study applied uniform pressure to We have devised a minicomputer-assisted method the digit on all sides viaan intermediate liner fabricated from of assessing perception of passive sinusoidal motion of a silicon gel material. the MCP and MTP joints in man, utilizing a modified A minicomputer was programmed to run the experiment von Bekksy procedure similar to that used in au- as well as to record and sort data. An identifyingnumber; the diometry [22]. We believe that a reliable and precise subject’sage, sex, and handedness; the joint to be tested; the quantitation technique is necessary as a first step in date; and the number of trials used were entered by tele-

From the Departments of and of Electrical and Com- ALcepted for publication May 20, 1977. puter Engineering, University of Michigan Medical Center, Ann Arbor, MI. Address reprint requests to Dr Kokmen, University of Michigan Medical Center, Ann Arbor, MI 48 109.

279 typewriter and stored in computer disc files. The threshold sensation. The subject was instructed to release the finger stimulus intensity in degrees, the frequency of stimulation, from the switch when the sensation of movement was lost, and summary statistics concerning the response of the sub- and the amplitude of the stimulus was then increased once jects were also stored in the disc file. A block diagram of the more. In this way, it was possible to obtain a series of upper system is shown in Figure 1. and lower thresholds of sensation of movement for each Fourteen normal test subjects, 6 women and 8 men, were digit, This is similar to von BikPsy’s audiometric method recruited from co-workers, acquaintances, and students. [22]. The actual threshold was assumed to be the level of The age range was from 18 to 29 years with a median of 23 stimulus intensity above which the subject detected move- and a mean of 22.2 years. Thirteen subjects were right- ment more than 50% of the time. Precise measurement of handed and 1 was left-handed. This was the first testing of the stimulus intensity was accomplished electronically and this type for each of the subjects; personnel who had been recorded by the computer whenever the subject responded involved in the development of the apparatus and had tested by moving his finger to or from the switch. and retested themselves were excluded from the study To acquaint the subject with the testing procedure and group. the sensations he might be experiencing, a trial test on the The subjects were seated comfortably in a dimly lit room. right index finger was carried out before data gathering was They extended their extremity to be tested into the ap- begun. At the end of the trial test, another conversation paratus (Fig 2). A cloth drape was positioned over the hand session was held with the subject to answer questions or or foot to exclude vision. The digit to be tested was isolated clarify points. The results of this trial test were not included from the others by gently applied cloth straps, and the in the final data reported. extremity was supported (Fig 2, inset). A standardized para- For each digit tested, seven pairs of threshold estimates graph stating the goals and procedures of the experiment were obtained at test frequencies of 0.5 and 5.0 Hz. The first was read aloud, and the subject was given the opportunity to two pairs were discarded to reduce or eliminate carryover ask questions before testing was begun. from a previous test frequency, and the remaining five The joint to be tested was passively flexed and extended measurements were used for all calculations. The testing in a sinusoidal fashion; these sinusoidal stimuli were varied time was approximately 15 minutes for each digit tested, in intensity and frequency. The digit to be tested was on the thus requiring approximately 90 minutes for the completion same plane as the palmar surface of the hand or the plantar of an experiment for a given subject. This included surface of the foot at the beginning of the experiment. For a changeover time between digits. given frequency, the stimulus intensity gradually increased from zero to a maximum of 10 degrees of total motion of the Results joint. The sinusoid stimulus was applied continuously and The Table gives a sample listing of the data from one was slowly increased in intensity until perceived by the digit, including the mean value of upper, lower, and subject. The subjects were instructed to concentratc on a actual thresholds as well as the standard deviations for sense of motion of the digit and were asked to indicate the each frequency tested. A coefficient of variation ob- earliest perception of movement by placing a finger of tained by multiplying the standard deviation by 100 the other hand on a specially designed response switch. and dividing the result by the mean is also shown. A When the subject indicated perception of movement by listing each data point is also included. pressing the response switch, the stimulus amplitude was of gradually decreased until it was below the threshold for Fig 1. Diagram of the testing and recording apparatus.

TELETYPE WRITER SYSTEM PRINTER DATA PROCESSING DATA OUTPUT AND STORAGE

DIGITAL POSITION

MECHANICAL ACTUATOR SERVO CONTROLLER SUBJECT AND CONTROLLED UNDER . COMPUTER BY THE TEST RESPONSE INTERFACE SERVO SYSTEM SWITCH CIRCUITS A

i

280 Annals of Neurology Vol 2 No 4 October 1977 Fig 2.1 ‘be te.rting apparatus, .rhowing nreihmiral assembly. Inset shoico subject? irrdex.frnger in place.

Sample of Azuzlable Computer Data jw Each Dtgit ‘Ierted Female 22 years hght-handed Right index finger

Upper Threshold Lower Threshold Threshold Frequency M SI) cv M SD cv M SD cv 0.5 1.05 0.07 6.67 0.52 0.06 11.54 0.70 0.05 6.33 5.0 0.54 0.04 7.40 0.35 0.03 8.57 0.45 0.02 4.44 Individual data points for the above means for upper and lower thresholds:

Frequency = 0.5 Hz Response No. IJpprr Threshold Louier Threshold 1 1.17 0.57 L 1.02 0.48 3 1.00 0.60 4 1.02 0.52 5 1.05 0.4 5 Frequency = 5.0 Hz Response No. Upper Threshold Lower Threshold 1 0.57 0.31 2 0.48 0.36 3 0.52 0.36 4 0.57 0.38 5 0.5 5 0.36

M = mean, expressed in degrees of peak sinusoidal displacement of linger; SD = standard deviation; CV = coefficient of variation. We have elected to use sinusoidal movements of digits as the set of defining stimuli. This, of course, is .._ not the only possible set, but the use of sinusoidal v) stimuli is attractive in several respects. Such stimuli W 2 0.8 have been profitably used in other sensory tests, nota- W W bly in audition and cutaneous sensation [22].In addi- n tion, a large quantity of data are already available on Ja 0.6 0 the response of joint receptors to sinusoidal stimuli in I v) animals [15, 24, 261. 2 0.4 I At the most peripheral level, receptors located in t joint capsule, muscle, tendon, or skin and subcutane- 0.2 ous tissue may be responsible for initiating the neurophysiological events that will terminate in per- ception of motion. For many years the view has pre- 0.5 HZ 5.0 HZ vailed that joint receptors more or less exclusively convey sensation [ 16, 181. Gold- Fig 3. Mean zdues undstandard deviution ofuueruge scheider [81 observed a blunting of motion sense thresholds in the 14 siibjects ftir euch of the six digits when electric current was applied to the region of the testedat 0.3 and 5.0 Hz. (RI = right index elbow joint. This led him to postulate that the recep- mrtarurptiphulungeul joint; LI = ieji index tors mediating this sensation must be located in the metucurptiphulangeul joint; RQ = quiriti mela- right joint capsule. When Browne, Lee, and Ring [2] in- rurpophulangeul joint; LQ = leji yuinti metucurpo- jected a local anesthetic into the joint capsule, 8 of phulungeul joint; RH = right hullux metutursophalungeal their subjects were unable to determine the position joint; LH = lejl hullux metatursophulungeul 9 joint.) of their great toe until extremes of range of movement were reached. Provins [20] anesthetized the proximal finger joint of his subjects and found that the angle of movement required to provoke sensation of motion Mean threshold values and standard deviation for rose from approximately 4 degrees (control group) to six digits of normal subjects at the two stimulation around 15 degrees (anesthetic group). Wyke [251 frequencies are shown in Figure 3. The threshold mentioned patients with difficulties of gait following value lies between 0.8 and 1 degree stimulus intensity damage to articular nerves. for each of the six joints tested at 0.5 Hz. At 5.0 Hz The role of receptors located in muscles has been the value is between 0.4 and 0.6 degree of stimulus investigated as well. Giaquinto et a1 [7] found no intensity. behavioral or encephalographic changes in sleeping A two-factor analysis of variance was performed on cats when group I muscle afferents were stimulated. the data to determine if differences between means Swett and Bourassa [21] were unable to condition cats could be attributed to naturally occurring experimen- to respond to stimulation of group I muscle afferents tal variation. The difference between high- and low- until they stimulated cutaneous afferents. Gelfan and frequency thresholds was significant at thep < 0.001 Carter [6] found that pulling on exposed muscle ten- level. When the thresholds obtained from the six dig- dons in man failed to evoke sensations of change in its at the same frequency were compared, there were muscle tension and joint position. While these no significant differences. findings suggest that muscle receptors do not contrib- ute to motion perception, another set of observations Discussion indicates a definite role for muscle afferents in posi- In 1826 Bell [I] proposed that proprioception, the tion sense and kinesthesia. In 1901 Pillsbury [191 sense of position of limbs in space, is a separate studied the knee joints with Goldscheider's methods. system, and the exact neurophysiological nature of He noted, however, that sensation was blunted when proprioception has been a matter of discussion since current was applied to the region of the tendons of the then. One of the problems in this area has been the muscles subserving the joints. When muscle as- rather vague definition of the terms position Jense, sociated with a particular joint is vibrated, systematic motion senre, and kinesthesia. For our purposes we will errors in position and judgment occur, and there is define position sense as the subjective appreciation of even perception of impossible limb positions [4, 91. a static or fixed joint sensation, and motion sense or When muscle afferents are preserved but joint affer- kinesthesia as the subjective appreciation of motion ents are paralyzed by either digital nerve block or around a joint. joint capsule anesthesia, appreciable kinesthesia and

282 Annals of Neurology Vol 2 No 4 October 1977 position sense remain [lo, 121. Surgical removal ofa quency. Rapidly adapting joint receptors do not re- joint does not abolish position sense [11]. spond to low-frequency sinusoidal stimuli but begin The role of skin receptors is more difficult to to respond feebly and occasionally at 0.1 to 0.2 Hz and evaluate. Digital nerves supply both skin and joints. are quickly provoked into increasingly powerful activ- We have been unsuccessful in our attempts to abolish ity above 1 Hz [24,261.The rapidly adapting afferents cutaneous sensation with topical anesthesia. Moberg project via the dorsal columns to the nucleus gracilis, [171 has addressed this problem. He states that: whereas present evidence indicates that S~OW~J~adapt- “blocking the joint receptors interferes with skin sen- ing joint afferents from hind limbs of cats and sation, and blocking cutaneous nerves will include the monkeys, at least, leave the dorsal columns at higher joint branches. The two factors cannot be separated in cervical levels [23, 241. This may have implications in this way” [17]. human perception of joint motion at different fre- It has been suggested that type I1 mechanorecep- quencies. tors in the skin may be able to function as propriocep- Our study does not furnish conclusive data that tors [131. This type of cutaneous receptor responds would clarify the issue of which elements of the readily to skin stretching as well as to pressure on the peripheral contribute to perception of skin. If cutaneous receptors do contribute to pro- motion. However, availability of this reliable, easily prioception, type I1 mechanoreceptors are the most tolerated, precise method of quantitation is a neces- likely candidates for the role. Chambers et a1 [3] dis- sary first step in pspchophysical or psychophysiologi- count the possibility of a proprioceptive role for type cal studies of kinesthesia. 11 mechanoreceptors on the basis that adjacent units do not always respond in the same way to a particular Supported in part by US Public Health Service Grant NSO 8470. movement of the limb in cats. When Browne, Lee, and Ring [2] anesthetized the joint capsule of the great References toe, the toe could be passed through its full range of 1. Bell C: On the nervous circle that connecrs voluntary muscles movement either upward or downward. The subjects with the brain. PhilTrans K Soc LondPart III:163-173, 1826 failed to detect movement even when the joint had 2. Browne K, Lee J, Ring PA: The sensation of the passive been moved through its full range. Ultimately, when movement at the metatarsophalangral joint of the great toe in man. J Physiol (Lond) 126:448-458, 1954 the extreme of movement was reached, the subjects 3. Chambers MR, Andrcs KH, Duering MV, et al: The structure were able to detect the position of the toe, presumably and function of the slowly adapting type I1 mechanoreceptors by means of the sensations generated by skin stretch- in hairy skin. J Exp Psycho1 57:417-415, 1972 ing on the dorsal or volar surface of the joint. If these 4. Craske B: Perception of impossible limb positions induced by observations are correct, it would seem that cutaneous tendon vibration. Science l96:7 1-73, 1777 5. Dyck PJ: Quantitation of cutaneous sensation in man, in Dyck receptors could not play a major role in provoking the PJ, Thomas PK, Lambert EF (eds): Peripheral Neuropathy. threshold sensations obtained in our experiments Philadelphia, WB Saunders CoInpany, 1975 since only small, midrange movements took place. It 6. Gelfan S, Carter S: Muscle sense in man. Exp Neurol 18:469- is not entirely certain that anesthetic action remained 473, 1967 exclusively in the joint capsule in the experiments of 7. Giaquinto S, Pompeiano 0, Swett JE: EEG and behavioral effecrs of fore- and hindlimb muscular afferent volleys in Browne et al, however. unrestrained cats. Arch Ital Biol 101:133-118, 1963 Our results appear to be quite uniform and repro- 8. Goldschcider A: Untersuchungen iiber den Muskelsinn. Arch ducible from subject to subject and can be used as a Anat Physiol Leipzig Physiol Abteil 1889, pp 369-503 reliable means of measuring motion sense, at least in Y. Goodwin GM, McCloskey DI, Matthews PBC: Proprioceprive the joints we tested. The thresholds of motion we illusions induced by muscle vibration: contribution by muscle spindles to perception. Science 175:1382-1384, 1972 obtained are smaller than those reported by 10. Goodwin GM, McCloskey D1, Matthews PBC: The persis- Goldscheider, Browne et al, and Provins, who all used tcnce of appreciable kinesthesia after paralyzing joint afferents constant-velocity measurements. Since we used but preservingmusck afferents. Brain Res 37:326-329, 1972 sinusoidal stimuli, the results should not be compara- 11. Grigg P, Finerman GA, Riley LH: Joint position sense after ble in the strictest sense. We found much less varia- total hip replacement.JBone Joint Surg [Am] 55:1016-1025, 1973 tion from subject to subject than did Browne et al. 12. Horch KW, Clark FJ, Burgess PR: Awareness of knee joint In studies of various receptor types responding to angle under static conditions. J Neurophysiol 38: 1436-1447. motion of the hind limb joints of cats, McCall et a1 [I51 1975 found that slowly adapting receptors recorded from 13. Knibestd M, Vallbo AB: Single unit analysis of mechano- the medial articular nerve readily follow sinusoidal receptor activity from humanglabrous skin. Acta Physiol Scand 80:178-195, 1970 stimuli at frequencies from below 0.001 Hz to at least 14. Laidlaw RW, Hamilton MA: The quantitative measurement of 7 Hz. The ability of these slowly adapting receptors to apperception of passive movement. NY Neurol Insc Bull follow sinusoidal stimuli increases slowly with fre- 6:145-171, 1937

Kukmen, Bussemeyer, and Williams: Digital hforion Perception 283 15. McCall WD Jr, Farias MAC, Williams WJ, et al: Static and with muscle and cutaneous nerve volleys in the cat. J dynamic responses of slowly adapting joint receptors. Brain Neurophysiol 30:530-545, 1967 Res 70:221-243, 1974 22. von BbkPsy G: Experiments in Hearing. New York, 16. Merton PA: Human position sense and sense of effort. Symp McGraw-Hill Book Company, 1960 Soc Exp Biol 18:187~-400,1964 23. Whitsel BL, Petrucelli LM, Shapiro G:Modality representa- 17. Moberg E: Fingers were made before forks. Hand 4:201-206, tion in the lumbar and cervical fasciculus gracilis of squirrel 1972 monkeys. Brain Res 15:67-78, 1969 18. Mountcastle VB: Medical Physiology, vol 2. St Louis, CV 24. Williams WJ, ReMent SL, Yin TCT, et al: Nucleus gracilis Mosby Company, 1968 responses to knee joint mocion: a frequency response study. 19. Pillsbury WB: Does the sensation ofmovement originate in the Brain Res 64:123-140, 1974 joints? Am J Physiol 12:346-353, 1901 25. Wyke B: The neurology of joints. Ann R Coll Surg Engl 20. Provins KA: The effect of peripheral nerve block on the 41:25--50, 1967 appreciation and execution of finger movements. J Physiol 26. Yin TCT, Willianis WJ: Dynamic response and transfer charac- (Lond) 143:55-67, 1058 teristics of joint in somatosensory thalamus of the cat. 21. Swert JE, Bourassa CM: Comparison of sensory thresholds J Nrurophysiol 39:582 -600, 1976

284 Annals of Neurology Vol 2 No 4 October 1977